Skip to main content
SpringerLink
Log in

Exploring the Extended Biological Functions of the Human Copper Chaperone of Superoxide Dismutase 1

  • Published:
The Protein Journal Aims and scope Submit manuscript

Abstract

The human copper chaperone of SOD1 (designated as CCS) was discovered more than two decades ago. It is an important copper binding protein and a homolog of Saccharomyces cerevisiae LYS7. To date, no studies have systematically or specifically elaborated on the functional development of CCS. This review summarizes the essential information about CCS, such as its localization, 3D structure, and copper binding ability. An emphasis is placed on its interacting protein partners and its biological functions in vivo and in vitro. Three-dimensional structural analysis revealed that CCS is composed of three domains. Its primary molecular function is the delivery of copper to SOD1 and activation of SOD1. It has also been reported to bind to XIAP, Mia40, and X11α, and other proteins. Through these protein partners, CCS is implicated in several vital biological processes in vivo, such as copper homeostasis, apoptosis, angiogenesis and oxidative stress. This review is anticipated to assist scientists in systematically understanding the latest research developments of CCS for facilitating the development of new therapeutics targeting CCS in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Culotta VC, Klomp LW, Strain J, Casareno RL, Krems B, Gitlin JD (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272(38):23469–23472

    Article  CAS  PubMed  Google Scholar 

  2. Bartnikas TB, Waggoner DJ, Casareno RL, Gaedigk R, White RA, Gitlin JD (2000) Chromosomal localization of CCS, the copper chaperone for Cu/Zn superoxide dismutase. Mamm Genome 11(5):409–411

    Article  CAS  PubMed  Google Scholar 

  3. Blockhuys S, Wittung-Stafshede P (2017) Roles of copper-binding proteins in breast cancer. Int J Mol Sci. https://doi.org/10.3390/ijms18040871

    Article  PubMed  PubMed Central  Google Scholar 

  4. Subramaniam JR, Lyons WE, Liu J, Bartnikas TB, Rothstein J, Price DL, Cleveland DW, Gitlin JD, Wong PC (2002) Mutant SOD1 causes motor neuron disease independent of copper chaperone-mediated copper loading. Nat Neurosci 5(4):301–307. https://doi.org/10.1038/nn823

    Article  CAS  PubMed  Google Scholar 

  5. Matson Dzebo M, Arioz C, Wittung-Stafshede P (2016) Extended functional repertoire for human copper chaperones. Biomol Concepts 7(1):29–39. https://doi.org/10.1515/bmc-2015-0030

    Article  CAS  PubMed  Google Scholar 

  6. Kim BE, Nevitt T, Thiele DJ (2008) Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 4(3):176–185. https://doi.org/10.1038/nchembio.72

    Article  CAS  PubMed  Google Scholar 

  7. Son M, Elliott JL (2014) Mitochondrial defects in transgenic mice expressing Cu,Zn superoxide dismutase mutations: the role of copper chaperone for SOD1. J Neurol Sci 336(1–2):1–7. https://doi.org/10.1016/j.jns.2013.11.004

    Article  CAS  PubMed  Google Scholar 

  8. Rae TD, Torres AS, Pufahl RA, O’Halloran TV (2001) Mechanism of Cu,Zn-superoxide dismutase activation by the human metallochaperone hCCS. J Biol Chem 276(7):5166–5176. https://doi.org/10.1074/jbc.M008005200

    Article  CAS  PubMed  Google Scholar 

  9. Caruano-Yzermans AL, Bartnikas TB, Gitlin JD (2006) Mechanisms of the copper-dependent turnover of the copper chaperone for superoxide dismutase. J Biol Chem 281(19):13581–13587. https://doi.org/10.1074/jbc.M601580200

    Article  CAS  PubMed  Google Scholar 

  10. Pope CR, De Feo CJ, Unger VM (2013) Cellular distribution of copper to superoxide dismutase involves scaffolding by membranes. Proc Natl Acad Sci USA 110(51):20491–20496. https://doi.org/10.1073/pnas.1309820110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lamb AL, Wernimont AK, Pufahl RA, Culotta VC, O’Halloran TV, Rosenzweig AC (1999) Crystal structure of the copper chaperone for superoxide dismutase. Nat Struct Biol 6(8):724–729. https://doi.org/10.1038/11489

    Article  CAS  PubMed  Google Scholar 

  12. Schmidt PJ, Ramos-Gomez M, Culotta VC (1999) A gain of superoxide dismutase (SOD) activity obtained with CCS, the copper metallochaperone for SOD1. J Biol Chem 274(52):36952–36956

    Article  CAS  PubMed  Google Scholar 

  13. Yim MB, Chock PB, Stadtman ER (1993) Enzyme function of copper, zinc superoxide dismutase as a free radical generator. J Biol Chem 268(6):4099–4105

    CAS  PubMed  Google Scholar 

  14. Lamb AL, Wernimont AK, Pufahl RA, O’Halloran TV, Rosenzweig AC (2000) Crystal structure of the second domain of the human copper chaperone for superoxide dismutase. Biochemistry 39(7):1589–1595

    Article  CAS  PubMed  Google Scholar 

  15. Endo T, Fujii T, Sato K, Taniguchi N, Fujii J (2000) A pivotal role of Zn-binding residues in the function of the copper chaperone for SOD1. Biochem Biophys Res Commun 276(3):999–1004. https://doi.org/10.1006/bbrc.2000.3581

    Article  CAS  PubMed  Google Scholar 

  16. Huppke P, Brendel C, Korenke GC, Marquardt I, Donsante A, Yi L, Hicks JD, Steinbach PJ, Wilson C, Elpeleg O, Moller LB, Christodoulou J, Kaler SG, Gartner J (2012) Molecular and biochemical characterization of a unique mutation in CCS, the human copper chaperone to superoxide dismutase. Hum Mutat 33(8):1207–1215. https://doi.org/10.1002/humu.22099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rothstein JD, Dykes-Hoberg M, Corson LB, Becker M, Cleveland DW, Price DL, Culotta VC, Wong PC (1999) The copper chaperone CCS is abundant in neurons and astrocytes in human and rodent brain. J Neurochem 72(1):422–429

    Article  CAS  PubMed  Google Scholar 

  18. Crapo JD, Oury T, Rabouille C, Slot JW, Chang LY (1992) Copper,zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc Natl Acad Sci USA 89(21):10405–10409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC (2001) A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276(41):38084–38089. https://doi.org/10.1074/jbc.M105296200

    Article  CAS  PubMed  Google Scholar 

  20. Geller BL, Winge DR (1982) Rat liver Cu,Zn-superoxide dismutase. Subcellular location in lysosomes. J Biol Chem 257(15):8945–8952

    CAS  PubMed  Google Scholar 

  21. Keller GA, Warner TG, Steimer KS, Hallewell RA (1991) Cu,Zn superoxide dismutase is a peroxisomal enzyme in human fibroblasts and hepatoma cells. Proc Natl Acad Sci USA 88(16):7381–7385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Schmidt PJ, Kunst C, Culotta VC (2000) Copper activation of superoxide dismutase 1 (SOD1) in vivo. Role for protein-protein interactions with the copper chaperone for SOD1. J Biol Chem 275(43):33771–33776. https://doi.org/10.1074/jbc.M006254200

    Article  CAS  PubMed  Google Scholar 

  23. Wong PC, Waggoner D, Subramaniam JR, Tessarollo L, Bartnikas TB, Culotta VC, Price DL, Rothstein J, Gitlin JD (2000) Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 97(6):2886–2891. https://doi.org/10.1073/pnas.040461197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Beckman JS, Esetvez AG, Barbeito L, Crow JP (2002) CCS knockout mice establish an alternative source of copper for SOD in ALS. Free Radic Biol Med 33(10):1433–1435. https://doi.org/10.1016/S0891-5849(02)01092-4

    Article  CAS  PubMed  Google Scholar 

  25. Casareno RL, Waggoner D, Gitlin JD (1998) The copper chaperone CCS directly interacts with copper/zinc superoxide dismutase. J Biol Chem 273(37):23625–23628

    Article  CAS  PubMed  Google Scholar 

  26. Lamb AL, Torres AS, O’Halloran TV, Rosenzweig AC (2001) Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat Struct Biol 8(9):751–755. https://doi.org/10.1038/nsb0901-751

    Article  CAS  PubMed  Google Scholar 

  27. Torres AS, Petri V, Rae TD, O’Halloran TV (2001) Copper stabilizes a heterodimer of the yCCS metallochaperone and its target superoxide dismutase. J Biol Chem 276(42):38410–38416. https://doi.org/10.1074/jbc.M104790200

    Article  CAS  PubMed  Google Scholar 

  28. Banci L, Bertini I, Cantini F, Kozyreva T, Massagni C, Palumaa P, Rubino JT, Zovo K (2012) Human superoxide dismutase 1 (hSOD1) maturation through interaction with human copper chaperone for SOD1 (hCCS). Proc Natl Acad Sci USA 109(34):13555–13560. https://doi.org/10.1073/pnas.1207493109

    Article  PubMed  PubMed Central  Google Scholar 

  29. Zhu H, Shipp E, Sanchez RJ, Liba A, Stine JE, Hart PJ, Gralla EB, Nersissian AM, Valentine JS (2000) Cobalt(2+) binding to human and tomato copper chaperone for superoxide dismutase: implications for the metal ion transfer mechanism. Biochemistry 39(18):5413–5421

    Article  CAS  PubMed  Google Scholar 

  30. Mufti AR, Burstein E, Duckett CS (2007) XIAP: cell death regulation meets copper homeostasis. Arch Biochem Biophys 463(2):168–174. https://doi.org/10.1016/j.abb.2007.01.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC, Salvesen GS (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104(5):791–800

    Article  CAS  PubMed  Google Scholar 

  32. Huang Y, Park YC, Rich RL, Segal D, Myszka DG, Wu H (2001) Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain. Cell 104(5):781–790

    CAS  PubMed  Google Scholar 

  33. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES, Shi Y (2001) Structural basis of caspase-7 inhibition by XIAP. Cell 104(5):769–780

    Article  CAS  PubMed  Google Scholar 

  34. Lewis J, Burstein E, Reffey SB, Bratton SB, Roberts AB, Duckett CS (2004) Uncoupling of the signaling and caspase-inhibitory properties of X-linked inhibitor of apoptosis. J Biol Chem 279(10):9023–9029. https://doi.org/10.1074/jbc.M312891200

    Article  CAS  PubMed  Google Scholar 

  35. Birkey Reffey S, Wurthner JU, Parks WT, Roberts AB, Duckett CS (2001) X-linked inhibitor of apoptosis protein functions as a cofactor in transforming growth factor-beta signaling. J Biol Chem 276(28):26542–26549. https://doi.org/10.1074/jbc.M100331200

    Article  CAS  PubMed  Google Scholar 

  36. Levkau B, Garton KJ, Ferri N, Kloke K, Nofer JR, Baba HA, Raines EW, Breithardt G (2001) xIAP induces cell-cycle arrest and activates nuclear factor-kappaB: new survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells. Circ Res 88(3):282–290

    Article  CAS  PubMed  Google Scholar 

  37. Hofer-Warbinek R, Schmid JA, Stehlik C, Binder BR, Lipp J, de Martin R (2000) Activation of NF-kappa B by XIAP, the X chromosome-linked inhibitor of apoptosis, in endothelial cells involves TAK1. J Biol Chem 275(29):22064–22068. https://doi.org/10.1074/jbc.M910346199

    Article  CAS  PubMed  Google Scholar 

  38. Sanna MG, da Silva Correia J, Luo Y, Chuang B, Paulson LM, Nguyen B, Deveraux QL, Ulevitch RJ (2002) ILPIP, a novel anti-apoptotic protein that enhances XIAP-mediated activation of JNK1 and protection against apoptosis. J Biol Chem 277(34):30454–30462. https://doi.org/10.1074/jbc.M203312200

    Article  CAS  PubMed  Google Scholar 

  39. Sanna MG, Duckett CS, Richter BW, Thompson CB, Ulevitch RJ (1998) Selective activation of JNK1 is necessary for the anti-apoptotic activity of hILP. Proc Natl Acad Sci USA 95(11):6015–6020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Mufti AR, Burstein E, Csomos RA, Graf PC, Wilkinson JC, Dick RD, Challa M, Son JK, Bratton SB, Su GL, Brewer GJ, Jakob U, Duckett CS (2006) XIAP Is a copper binding protein deregulated in Wilson’s disease and other copper toxicosis disorders. Mol Cell 21(6):775–785. https://doi.org/10.1016/j.molcel.2006.01.033

    Article  CAS  PubMed  Google Scholar 

  41. Brady GF, Galban S, Liu X, Basrur V, Gitlin JD, Elenitoba-Johnson KS, Wilson TE, Duckett CS (2010) Regulation of the copper chaperone CCS by XIAP-mediated ubiquitination. Mol Cell Biol 30(8):1923–1936. https://doi.org/10.1128/MCB.00900-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121(7):1059–1069. https://doi.org/10.1016/j.cell.2005.04.011

    Article  CAS  PubMed  Google Scholar 

  43. Banci L, Bertini I, Cefaro C, Cenacchi L, Ciofi-Baffoni S, Felli IC, Gallo A, Gonnelli L, Luchinat E, Sideris D, Tokatlidis K (2010) Molecular chaperone function of Mia40 triggers consecutive induced folding steps of the substrate in mitochondrial protein import. Proc Natl Acad Sci USA 107(47):20190–20195. https://doi.org/10.1073/pnas.1010095107

    Article  PubMed  PubMed Central  Google Scholar 

  44. Reddehase S, Grumbt B, Neupert W, Hell K (2009) The disulfide relay system of mitochondria is required for the biogenesis of mitochondrial Ccs1 and Sod1. J Mol Biol 385(2):331–338. https://doi.org/10.1016/j.jmb.2008.10.088

    Article  CAS  PubMed  Google Scholar 

  45. Kloppel C, Suzuki Y, Kojer K, Petrungaro C, Longen S, Fiedler S, Keller S, Riemer J (2011) Mia40-dependent oxidation of cysteines in domain I of Ccs1 controls its distribution between mitochondria and the cytosol. Mol Biol Cell 22(20):3749–3757. https://doi.org/10.1091/mbc.E11-04-0293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gross DP, Burgard CA, Reddehase S, Leitch JM, Culotta VC, Hell K (2011) Mitochondrial Ccs1 contains a structural disulfide bond crucial for the import of this unconventional substrate by the disulfide relay system. Mol Biol Cell 22(20):3758–3767. https://doi.org/10.1091/mbc.E11-04-0296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154(6):1380–1389. https://doi.org/10.1016/j.cell.2013.08.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Narindrasorasak S, Zhang X, Roberts EA, Sarkar B (2004) Comparative analysis of metal binding characteristics of copper chaperone proteins, Atx1 and ATOX1. Bioinorg Chem Appl. https://doi.org/10.1155/S1565363304000081

    Article  PubMed  PubMed Central  Google Scholar 

  49. Muller PA, Klomp LW (2009) ATOX1: a novel copper-responsive transcription factor in mammals? Int J Biochem Cell Biol 41(6):1233–1236. https://doi.org/10.1016/j.biocel.2008.08.001

    Article  CAS  PubMed  Google Scholar 

  50. Itoh S, Kim HW, Nakagawa O, Ozumi K, Lessner SM, Aoki H, Akram K, McKinney RD, Ushio-Fukai M, Fukai T (2008) Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation. J Biol Chem 283(14):9157–9167. https://doi.org/10.1074/jbc.M709463200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Petzoldt S, Kahra D, Kovermann M, Dingeldein AP, Niemiec MS, Aden J, Wittung-Stafshede P (2015) Human cytoplasmic copper chaperones Atox1 and CCS exchange copper ions in vitro. Biometals 28(3):577–585. https://doi.org/10.1007/s10534-015-9832-1

    Article  CAS  PubMed  Google Scholar 

  52. Ohrvik H, Wittung-Stafshede P (2015) Identification of new potential interaction partners for human cytoplasmic copper chaperone Atox1: roles in gene regulation? Int J Mol Sci 16(8):16728–16739. https://doi.org/10.3390/ijms160816728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Biederer T, Cao X, Sudhof TC, Liu X (2002) Regulation of APP-dependent transcription complexes by Mint/X11s: differential functions of Mint isoforms. J Neurosci 22(17):7340–7351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. McLoughlin DM, Irving NG, Brownlees J, Brion JP, Leroy K, Miller CC (1999) Mint2/X11-like colocalizes with the Alzheimer's disease amyloid precursor protein and is associated with neuritic plaques in Alzheimer's disease. Eur J Neurosci 11(6):1988–1994

    Article  CAS  PubMed  Google Scholar 

  55. McLoughlin DM, Miller CC (1996) The intracellular cytoplasmic domain of the Alzheimer's disease amyloid precursor protein interacts with phosphotyrosine-binding domain proteins in the yeast two-hybrid system. FEBS Lett 397(2–3):197–200

    Article  CAS  PubMed  Google Scholar 

  56. Tanahashi H, Tabira T (1999) X11L2, a new member of the X11 protein family, interacts with Alzheimer’s beta-amyloid precursor protein. Biochem Biophys Res Commun 255(3):663–667. https://doi.org/10.1006/bbrc.1999.0265

    Article  CAS  PubMed  Google Scholar 

  57. Borg JP, Lopez-Figueroa MO, de Taddeo-Borg M, Kroon DE, Turner RS, Watson SJ, Margolis B (1999) Molecular analysis of the X11-mLin-2/CASK complex in brain. J Neurosci 19(4):1307–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. McLoughlin DM, Standen CL, Lau KF, Ackerley S, Bartnikas TP, Gitlin JD, Miller CC (2001) The neuronal adaptor protein X11alpha interacts with the copper chaperone for SOD1 and regulates SOD1 activity. J Biol Chem 276(12):9303–9307. https://doi.org/10.1074/jbc.M010023200

    Article  CAS  PubMed  Google Scholar 

  59. Nose Y, Rees EM, Thiele DJ (2006) Structure of the Ctr1 copper trans’PORE’ter reveals novel architecture. Trends Biochem Sci 31(11):604–607. https://doi.org/10.1016/j.tibs.2006.09.003

    Article  CAS  PubMed  Google Scholar 

  60. Dancis A, Haile D, Yuan DS, Klausner RD (1994) The Saccharomyces cerevisiae copper transport protein (Ctr1p). Biochemical characterization, regulation by copper, and physiologic role in copper uptake. J Biol Chem 269(41):25660–25667

    CAS  PubMed  Google Scholar 

  61. Prohaska JR (2008) Role of copper transporters in copper homeostasis. Am J Clin Nutr 88(3):826S–829S. https://doi.org/10.1093/ajcn/88.3.826S

    Article  CAS  PubMed  Google Scholar 

  62. Furukawa T, Komatsu M, Ikeda R, Tsujikawa K, Akiyama S (2008) Copper transport systems are involved in multidrug resistance and drug transport. Curr Med Chem 15(30):3268–3278

    Article  CAS  PubMed  Google Scholar 

  63. Hua H, Georgiev O, Schaffner W, Steiger D (2010) Human copper transporter Ctr1 is functional in Drosophila, revealing a high degree of conservation between mammals and insects. J Biol Inorg Chem 15(1):107–113. https://doi.org/10.1007/s00775-009-0599-0

    Article  CAS  PubMed  Google Scholar 

  64. Chang LY, Slot JW, Geuze HJ, Crapo JD (1988) Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J Cell Biol 107(6 Pt 1):2169–2179

    Article  CAS  PubMed  Google Scholar 

  65. Zuo X, Dong D, Sun M, Xie H, Kang YJ (2013) Homocysteine restricts copper availability leading to suppression of cytochrome C oxidase activity in phenylephrine-treated cardiomyocytes. PLoS One 8(6):e67549. https://doi.org/10.1371/journal.pone.0067549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Setty SR, Tenza D, Sviderskaya EV, Bennett DC, Raposo G, Marks MS (2008) Cell-specific ATP7A transport sustains copper-dependent tyrosinase activity in melanosomes. Nature 454(7208):1142–1146. https://doi.org/10.1038/nature07163

    Article  CAS  PubMed  Google Scholar 

  67. Kagan HM, Li W (2003) Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell. J Cell Biochem 88(4):660–672. https://doi.org/10.1002/jcb.10413

    Article  CAS  PubMed  Google Scholar 

  68. Ogra Y (2014) Molecular mechanisms underlying copper homeostasis in Mammalian cells. Nihon Eiseigaku Zasshi 69(2):136–145

    Article  CAS  PubMed  Google Scholar 

  69. Prohaska JR, Gybina AA (2004) Intracellular copper transport in mammals. J Nutr 134(5):1003–1006

    Article  CAS  PubMed  Google Scholar 

  70. Markossian KA, Kurganov BI (2003) Copper chaperones, intracellular copper trafficking proteins. Function, structure, and mechanism of action. Biochemistry (Mosc) 68(8):827–837

    Article  CAS  Google Scholar 

  71. Fukuoka M, Tokuda E, Nakagome K, Wu Z, Nagano I, Furukawa Y (2017) An essential role of N-terminal domain of copper chaperone in the enzymatic activation of Cu/Zn-superoxide dismutase. J Inorg Biochem 175:208–216. https://doi.org/10.1016/j.jinorgbio.2017.07.036

    Article  CAS  PubMed  Google Scholar 

  72. Wang L, Ge Y, Kang YJ (2016) Featured article: effect of copper on nuclear translocation of copper chaperone for superoxide dismutase-1. Exp Biol Med (Maywood) 241(14):1483–1488. https://doi.org/10.1177/1535370216645412

    Article  CAS  Google Scholar 

  73. Bertinato J, L’Abbe MR (2003) Copper modulates the degradation of copper chaperone for Cu, Zn superoxide dismutase by the 26 S proteosome. J Biol Chem 278(37):35071–35078. https://doi.org/10.1074/jbc.M302242200

    Article  CAS  PubMed  Google Scholar 

  74. Wang B, Dong D, Kang YJ (2013) Copper chaperone for superoxide dismutase-1 transfers copper to mitochondria but does not affect cytochrome c oxidase activity. Exp Biol Med (Maywood). https://doi.org/10.1177/1535370213497327

    Article  Google Scholar 

  75. West EC, Prohaska JR (2004) Cu,Zn-superoxide dismutase is lower and copper chaperone CCS is higher in erythrocytes of copper-deficient rats and mice. Exp Biol Med (Maywood) 229(8):756–764

    Article  CAS  Google Scholar 

  76. Suazo M, Olivares F, Mendez MA, Pulgar R, Prohaska JR, Arredondo M, Pizarro F, Olivares M, Araya M, Gonzalez M (2008) CCS and SOD1 mRNA are reduced after copper supplementation in peripheral mononuclear cells of individuals with high serum ceruloplasmin concentration. J Nutr Biochem 19(4):269–274. https://doi.org/10.1016/j.jnutbio.2007.04.003

    Article  CAS  PubMed  Google Scholar 

  77. Cozzolino M, Rossi S, Mirra A, Carri MT (2015) Mitochondrial dynamism and the pathogenesis of amyotrophic lateral sclerosis. Front Cell Neurosci 9:31. https://doi.org/10.3389/fncel.2015.00031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Renton AE, Chio A, Traynor BJ (2014) State of play in amyotrophic lateral sclerosis genetics. Nat Neurosci 17(1):17–23. https://doi.org/10.1038/nn.3584

    Article  CAS  PubMed  Google Scholar 

  79. Luchinat E, Barbieri L, Banci L (2017) A molecular chaperone activity of CCS restores the maturation of SOD1 fALS mutants. Sci Rep 7(1):17433. https://doi.org/10.1038/s41598-017-17815-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Abel O, Powell JF, Andersen PM, Al-Chalabi A (2012) ALSoD: A user-friendly online bioinformatics tool for amyotrophic lateral sclerosis genetics. Hum Mutat 33(9):1345–1351. https://doi.org/10.1002/humu.22157

    Article  CAS  PubMed  Google Scholar 

  81. Tokuda E, Furukawa Y (2016) Copper homeostasis as a therapeutic target in amyotrophic lateral sclerosis with SOD1 mutations. Int J Mol Sci. https://doi.org/10.3390/ijms17050636

    Article  PubMed  PubMed Central  Google Scholar 

  82. Kim HK, Chung YW, Chock PB, Yim MB (2011) Effect of CCS on the accumulation of FALS SOD1 mutant-containing aggregates and on mitochondrial translocation of SOD1 mutants: implication of a free radical hypothesis. Arch Biochem Biophys 509(2):177–185. https://doi.org/10.1016/j.abb.2011.02.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Greenough MA, Volitakis I, Li QX, Laughton K, Evin G, Ho M, Dalziel AH, Camakaris J, Bush AI (2011) Presenilins promote the cellular uptake of copper and zinc and maintain copper chaperone of SOD1-dependent copper/zinc superoxide dismutase activity. J Biol Chem 286(11):9776–9786. https://doi.org/10.1074/jbc.M110.163964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kato S, Sumi-Akamaru H, Fujimura H, Sakoda S, Kato M, Hirano A, Takikawa M, Ohama E (2001) Copper chaperone for superoxide dismutase co-aggregates with superoxide dismutase 1 (SOD1) in neuronal Lewy body-like hyaline inclusions: an immunohistochemical study on familial amyotrophic lateral sclerosis with SOD1 gene mutation. Acta Neuropathol 102(3):233–238

    CAS  PubMed  Google Scholar 

  85. Son M, Fu Q, Puttaparthi K, Matthews CM, Elliott JL (2009) Redox susceptibility of SOD1 mutants is associated with the differential response to CCS over-expression in vivo. Neurobiol Dis 34(1):155–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Corson LB, Strain JJ, Culotta VC, Cleveland DW (1998) Chaperone-facilitated copper binding is a property common to several classes of familial amyotrophic lateral sclerosis-linked superoxide dismutase mutants. Proc Natl Acad Sci USA 95(11):6361–6366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Wright GS, Antonyuk SV, Hasnain SS (2016) A faulty interaction between SOD1 and hCCS in neurodegenerative disease. Sci Rep 6:27691. https://doi.org/10.1038/srep27691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Stasser JP, Siluvai GS, Barry AN, Blackburn NJ (2007) A multinuclear copper(I) cluster forms the dimerization interface in copper-loaded human copper chaperone for superoxide dismutase. Biochemistry 46(42):11845–11856. https://doi.org/10.1021/bi700566h

    Article  CAS  PubMed  Google Scholar 

  89. Kawamata H, Manfredi G (2010) Import, maturation, and function of SOD1 and its copper chaperone CCS in the mitochondrial intermembrane space. Antioxid Redox Signal 13(9):1375–1384. https://doi.org/10.1089/ars.2010.3212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Huang P, Feng L, Oldham EA, Keating MJ, Plunkett W (2000) Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407(6802):390–395. https://doi.org/10.1038/35030140

    Article  CAS  PubMed  Google Scholar 

  91. Somwar R, Erdjument-Bromage H, Larsson E, Shum D, Lockwood WW, Yang G, Sander C, Ouerfelli O, Tempst PJ, Djaballah H, Varmus HE (2011) Superoxide dismutase 1 (SOD1) is a target for a small molecule identified in a screen for inhibitors of the growth of lung adenocarcinoma cell lines. Proc Natl Acad Sci USA 108(39):16375–16380. https://doi.org/10.1073/pnas.1113554108

    Article  PubMed  PubMed Central  Google Scholar 

  92. Papa L, Manfredi G, Germain D (2014) SOD1, an unexpected novel target for cancer therapy. Genes Cancer 5(1–2):15–21. https://doi.org/10.18632/genesandcancer.4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Qiu L, Ding X, Zhang Z, Kang YJ (2012) Copper is required for cobalt-induced transcriptional activity of hypoxia-inducible factor-1. J Pharmacol Exp Ther 342(2):561–567. https://doi.org/10.1124/jpet.112.194662

    Article  CAS  PubMed  Google Scholar 

  94. Wang J, Luo C, Shan C, You Q, Lu J, Elf S, Zhou Y, Wen Y, Vinkenborg JL, Fan J, Kang H, Lin R, Han D, Xie Y, Karpus J, Chen S, Ouyang S, Luan C, Zhang N, Ding H, Merkx M, Liu H, Chen J, Jiang H, He C (2015) Inhibition of human copper trafficking by a small molecule significantly attenuates cancer cell proliferation. Nat Chem 7(12):968–979. https://doi.org/10.1038/nchem.2381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bompiani KM, Tsai CY, Achatz FP, Liebig JK, Howell SB (2016) Copper transporters and chaperones CTR1, CTR2, ATOX1, and CCS as determinants of cisplatin sensitivity. Metallomics 8(9):951–962. https://doi.org/10.1039/c6mt00076b

    Article  CAS  PubMed  Google Scholar 

  96. Feng W, Ye F, Xue W, Zhou Z, Kang YJ (2009) Copper regulation of hypoxia-inducible factor-1 activity. Mol Pharmacol 75(1):174–182. https://doi.org/10.1124/mol.108.051516

    Article  CAS  PubMed  Google Scholar 

  97. Iskandar M, Swist E, Trick KD, Wang B, L’Abbe MR, Bertinato J (2005) Copper chaperone for Cu/Zn superoxide dismutase is a sensitive biomarker of mild copper deficiency induced by moderately high intakes of zinc. Nutr J 4:35. https://doi.org/10.1186/1475-2891-4-35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Bertinato J, Sherrard L, Plouffe LJ (2010) Decreased erythrocyte CCS content is a biomarker of copper overload in rats. Int J Mol Sci 11(7):2624–2635. https://doi.org/10.3390/ijms11072624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was funded by the following funds: National Science Foundation of China, Grant No. 81200115; Science and Technology Department of Sichuan Province project, Grants No. 2017HH0011; Municipal Government project of Chengdu Science and Technology Bureau, Grants No. 2016-XT00-00023-GX.

Author information

Authors and Affiliations

  1. Antibiotics Research and Re-evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, No. 168 Huaguan Road, Chenghua District, Chengdu, 610052, China

    Yan Ge, Lu Wang, Duanhua Li, Chen Zhao, Jinjun Li & Tao Liu

  2. International Phage Drug Research Center, Sichuan Industrial Institute of Antibiotics, Chengdu University, Chengdu, China

    Yan Ge, Lu Wang, Duanhua Li, Chen Zhao, Jinjun Li & Tao Liu

Authors
  1. Yan Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Duanhua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chen Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinjun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lu Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ge, Y., Wang, L., Li, D. et al. Exploring the Extended Biological Functions of the Human Copper Chaperone of Superoxide Dismutase 1. Protein J 38, 463–471 (2019). https://doi.org/10.1007/s10930-019-09824-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10930-019-09824-9

Keywords

Search

Navigation